Abstract
We analyzed the complete mitochondrial cytochrome b (cytb) gene and fragments of four nuclear loci: ApoB, RAG2, IRBP1 and BRCA1. These data allowed us to provide new insights into the diversity of the Asiatic water shrews of Indochina. A new, highly divergent genetic lineage of Chimarrogale was found in southern Vietnam, and this lineage included specimens from the provinces of Kon Tum, Dak Lak, and Lam Dong. Such finding represents the newest and southernmost records of Chimarrogale in Indochina. Morphological analysis classified the specimens from southern Vietnam as C. varennei proper, which is restricted to that region, whereas the polymorphic C. himalayica, which contained at least four cytochrome b haplogroups, occurred in central and northern Vietnam and southern China. This distinct C. varennei lineage closely related to the C. platycephalus + C. leander clade suggests the existence of an unknown glacial refuge in Tay Nguyen Plateau, southern Vietnam. Because the Bornean C. phaeura (i) was sister-group of the rest of Chimarrogale sensu lato and (ii) had a high genetic divergence (~15% for cytochrome b) and geographical isolation, we suggest that C. phaeura be placed into a separate genus, Crossogale Thomas, 1921. This genus should also include C. sumatrana (Sumatra) and C. hantu (Peninsular Malaysia). On those grounds, we propose a new classification system for Asiatic water shrews.
References
Abramov, A.V., Can, D.N., Hai, B.T. & Son, N.T. (2013) An annotated checklist of the insectivores (Mammalia, Lipotyphla) of Vietnam. Russian Journal of Theriology, 12, 57–70.
Anderson, J. (1877) Description of some new and little known Asiatic shrew in the Indian Museum, Calcutta. Journal of the Asiatic Society of Bengal, 46 (3), 261–283.
Anthony, H.E. (1941) Mammals collected by the Vernay-Cutting Burma expedition. Field Museum of Natural History, Zoology Series, 27, 37–125.
Balakirev, A.E., Abramov, A.V. & Rozhnov, V.V. (2013) Revision of the genus Leopoldamys (Rodentia, Muridae) as inferred from morphological and molecular data, with a special emphasis on the species composition in continental Indochina. Zootaxa, 3640 (4), 521–549.
https://doi.org/10.11646/zootaxa.3640.4.2Bannikova, A.A., Abramov, A.V., Borisenko, A.V., Lebedev, V.S. & Rozhnov, V.V. (2011) Mitochondrial diversity of the white-toothed shrews (Mammalia, Eulipotyphla, Crocidura) in Vietnam. Zootaxa, 2812, 1–20.
Borisenko, A.V., Kruskop, S.V. & Ivanova, N.V. (2009) A new mouse-eared bat (Mammalia: Chiroptera: Vespertilionidae) from Vietnam. Russian Journal of Theriology, 7, 57–69.
Carstens, B.C., Pelletier, T.A., Reid, N.M. & Satler, J.D. (2013) How to fail at species delimitation. Molecular Ecology, 22, 4369–4383.
https://doi.org/10.1111/mec.12413Corbet, G.B. & Hill, J.E. (1992) The Mammals of the Indo-Malayan Region: a Systematic Review. Oxford University Press, Oxford, 488 pp.
De Winton, W.E. (1899) On Chinese mammals, principally from Western Sechuen. Proceedings of the Zoological Society of London, 1899 (1), 572–578.
https://doi.org/10.1111/j.1469-7998.1899.tb06875.xEames, J.C. (1995) Endemic birds and protected area development on the Da Lat plateau, Vietnam. Bird Conservation International, 5, 491–523.
https://doi.org/10.1017/S0959270900001209Esselstyn, J.A. & Brown, R.M. (2009) The role of repeated sea-level fluctuations in the generation of shrew (Soricidae: Crocidura) diversity in the Philippine Archipelago. Molecular Phylogenetics and Evolution, 53, 171–181.
https://doi.org/10.1016/j.ympev.2009.05.034Francis, C.M. (2008) A Field Guide to the Mammals of South-East Asia. New Holland, London, 392 pp.
Gray, J.E. (1842) Description of some new genera and fifty unrecorded species of Mammalia. Annals and Magazine of Natural History, 10, 255–267.
https://doi.org/10.1080/03745484209445232Hall, T.A. (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Harrison, J.L. (1958) Chimarrogale hantu a new water shrew from the Malay Peninsula, with a note on the genera Chimarrogale and Crossogale (Insectivora, Soricidae). Annals and Magazine of Natural History, Series 13, 1 (4), 282–290.
https://doi.org/10.1080/00222935808650947Hoffmann, R.S. (1987) A review of the systematics and distribution of Chinese red-toothed shrews (Mammalia: Soricinae). Acta Theriologica Sinica, 7, 100–139.
Hoffmann, R.S. & Lunde, D. (2008) Order Soricomorpha. In: Smith, A.T. & Xie, Y. (Eds.), A Guide to the Mammals of China. Princeton University Press, Princeton & Oxford, pp. 297–327.
Hutterer, R. (2005) Order Soricomorpha. In: Wilson, D.E. & Reeder, D.M. (Eds.), Mammals Species of the World. A Taxonomic and Geographic Reference. 3rd Edition. The Johns Hopkins University Press, Baltimore, pp. 220–311.
Jenkins, P.D., Abramov, A.V., Rozhnov, V.V. & Makarova, O.V. (2007) Description of two new species of white-toothed shrews belonging to the genus Crocidura (Soricomorpha: Soricidae) from the Ngoc Linh Mountain, Vietnam. Zootaxa, 1589, 57–68.
Jobb, G. (2008) TREEFINDER, version of October 2008. Munich, Germany. Distributed by the author. Available from: http://www.treefinder.de (accessed 17 January 2017)
Jones, G.S. & Mumford, R.E. (1971) Chimarrogale from Taiwan. Journal of Mammalogy, 52, 228–232.
https://doi.org/10.2307/1378458Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
https://doi.org/10.1007/BF01731581Kruskop, S.V. & Eger, J.L. (2008) A new species of tube-nosed bat Murina (Vespertilionidae, Chiroptera) from Vietnam. Acta Chiropterologica, 10, 213–220.
https://doi.org/10.3161/150811008X414809Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
https://doi.org/10.1093/molbev/mss020Meschersky, I.G., Abramov, A.V., Lebedev, V.S., Chichkina, A.N. & Rozhnov, V.V. (2016) Evidence of a complex phylogeographic structure in the Indomalayan pencil-tailed tree mouse Chiropodomys gliroides (Rodentia: Muridae) in eastern Indochina. Biochemical Systematics and Ecology, 65, 147–157.
https://doi.org/10.1016/j.bse.2016.02.015Motokawa, M., Harada, M., Apin, L., Yasuma, S., Yuan, S.-L. & Lin, L.-K. (2006) Taxonomic study of the water shrews Chimarrogale himalayica and C. platycephala. Acta Theriologica, 51 (2), 215–223.
https://doi.org/10.1007/BF03192673Nazarov, R.A., Orlov, N.L., Sang, N.N. & Ho, T.C. (2008) Taxonomy of naked-toes geckos Cyrtodactylus irregularis complex of south Vietnam and description of a new species from Chu Yang Sin National Park (Krong Bong District, Dac Lac Province, Vietnam). Russian Journal of Herpetology, 15, 141–156.
Ngo, V.T. & Bauer, A.M. (2008) Descriptions of two new species of Cyrtodactylus Gray, 1827 (Squamata: Gekkonidae) endemic to southern Vietnam. Zootaxa, 1715, 27–42.
Ngo, V.T., Bauer, A.M., Wood, P.L. Jr. & Grismer, J.L. (2009) A new species of Gekko Laurenti, 1768 (Squamata, Gekkonidae) from Dong Nai Province, Southeastern Vietnam. Zootaxa, 2238, 33–42.
Ohdachi, S., Dokuchaev, N.E., Hasegawa, M. & Masuda, R. (2001) Intraspecific phylogeny and geographical variation of six species of northeastern Asiatic Sorex shrews based on the mitochondrial cytochrome b sequences. Molecular Ecology, 10, 2199–2213.
https://doi.org/10.1046/j.1365-294X.2001.01359.xOsgood, W.H. (1932) Mammals of the Kelley-Roosevelts and Delacour Asiatic expeditions. Field Museum of Natural History, Zoological Series, 18, 193–339.
Orlov, N.L., Sang, N.N. & Ho, T.C. (2010) Description of a new species and new records of Rhacophorus genus (Amphibia: Anura: Rhacophoridae) with the review of amphibians and reptiles diversity of Chu Yang Sin National Park (Dac Lac Province, Vietnam). Russian Journal of Herpetology, 15, 67–84.
Rambaut, A. & Drummond, A. (2005) Tracer version 1.5. Computer program distributed by the authors. Department of Zoology, University of Oxford, UK. Available from: http://http://evolve.zoo.ox.ac.uk/software.html (accessed 17 January 2017)
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180Rowley, J.J.L., Le, T.T.D., Tran, T.A.D., Stuart, B.L. & Hoang, D.H. (2010) A new tree frog of the genus Rhacophorus (Anura: Rhacophoridae) from southern Vietnam. Zootaxa, 2727, 45–55.
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Lab. Press, New York, 256 pp.
Stuart, B.L., Rowley, J.J.L., Tran, D.T.A., Le, D.T.T. & Hoang, H.D. (2011) The Leptobrachium (Anura: Megophryidae) of the Langbian Plateau, southern Vietnam, with description of a new species. Zootaxa, 2804, 25–40.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.
https://doi.org/10.1093/molbev/msr121Temminck, C.J. (1842) Aperçu général et spécifique sur les mammiféres qui habitent le Japon et les iles qui en dépendent. In: Siebold, P.F., Temminck, C.J. & Schlegel, H. (Eds.), Fauna Japonica. Ex Officin. lithogr. ab A. Arnz & Soc., Lugduni Batavorum, pp.1–24.
Thomas, O. (1898) Descriptions of new Bornean and Sumatran mammals. Annals and Magazine of Natural History, Series 7, 2 (9), 245–251.
https://doi.org/10.1080/00222939808678039Thomas, O. (1902) On two mammals from China. Annals and Magazine of Natural History, Series 7, 10 (56), 163–166.
Thomas, O. (1921) On a new genus and species of shrew, and some new Muridae from the East-Indian Archipelago. Annals and Magazine of Natural History, 9 (7), 243–249.
https://doi.org/10.1080/00222932108632519Thomas, O. (1927) The Delacour exploration of French Indo-China—Mammals. Proceedings of the Zoological Society of London, 97 (1), 41–58.
https://doi.org/10.1111/j.1096-3642.1927.tb02245.xTordoff, A.W. (Ed.) (2002) Directory of Important Bird Areas in Vietnam: Key Sites for Conservation. BirdLife International in Indochina and Institute of Ecology and Biological Resources, Hanoi, 233 pp.
Yuan, S.-L., Jiang, X.-L., Li, Z.-J., He, K., Harada, M., Oshida, T. & Lin, L.-K. (2013) A mitochondrial phylogeny and biogeographical scenario for Asiatic water shrews of the genus Chimarrogale: implications for taxonomy and low-latitude migration routes. PLoS ONE, 8 (10), e77156.
https://doi.org/10.1371/journal.pone.0077156Zemlemerova, E.D., Bannikova, A.A., Lebedev, V.S., Rozhnov, V.V. & Abramov, A.V. (2016) Secrets of the underground Vietnam: an underestimated species diversity of Asian moles (Lipotyphla: Talpidae: Euroscaptor). Proceedings of the Zoological Institute RAS, 320 (2), 193–220.